Early detection of nerve fiber loss by corneal confocal microscopy and skin biopsy in recently diagnosed type 2 diabetes

Diabetes

Volumn 63, Issue 7, 2014, Pages 2454-2463

  Ziegler, Dan ^a,b   Papanas, Nikolaos ^a   Zhivov, Andrey ^c   Allgeier, Stephan ^d   Winter, Karsten ^e   Ziegler, Iris ^a   Brüggemann, Jutta ^a   Strom, Alexander ^a   Peschel, Sabine ^c   Köhler, Bernd ^d   Stachs, Oliver ^c   Guthoff, Rudolf F ^c   Roden, Michael ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

^d KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^e UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ALGORITHM; ARTICLE; AUTONOMIC NERVE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIABETIC PATIENT; FEMALE; FUNCTION TEST; HEART RATE VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NERVE CONDUCTION; NERVE FIBER; NERVE INJURY; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL NERVE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SKIN; SKIN BIOPSY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; BIOPSY; CASE-CONTROL STUDIES; CORNEA; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; DIABETIC RETINOPATHY; DIAGNOSTIC TECHNIQUES, OPHTHALMOLOGICAL; EARLY DIAGNOSIS; FEMALE; HUMANS; MALE; MICROSCOPY, CONFOCAL; MIDDLE AGED; NERVE FIBERS; SKIN; YOUNG ADULT;

EID: 84903216018     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1819     Document Type: Article

References (41)

1. Dyck PJ, Albers JW, Andersen H, et al.; on behalf of the Toronto Expert Panel on Diabetic Neuropathy. Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev 2011;27:620-628
2. Malik R, Veves A, Tesfaye S, et al.; on behalf of the Toronto Consensus Panel on Diabetic Neuropathy. Small fiber neuropathy: role in the diagnosis of diabetic sensorimotor polyneuropathy. Diabetes Metab Res Rev 2011;27:678-684
3. Rosenberg ME, Tervo TM, Immonen IJ, Müller LJ, Grönhagen-Riska C, Vesaluoma MH. Corneal structure and sensitivity in type 1 diabetes mellitus. Invest Ophthalmol Vis Sci 2000;41:2915-2921
4. Malik RA, Kallinikos P, Abbott CA, et al. Corneal confocal microscopy: a non-invasive surrogate of nerve fibre damage and repair in diabetic patients. Diabetologia 2003;46:683-688 (Pubitemid 36808188)
5. Zhivov A, Blum M, Guthoff R, Stachs O. Real-time mapping of the subepithelial nerve plexus by in vivo confocal laser scanning microscopy. Br J Ophthalmol 2010;94:1133-1135
6. Papanas N, Ziegler D. Corneal confocal microscopy: a new technique for early detection of diabetic neuropathy. Curr Diab Rep 2013;13:488-499
7. Hertz P, Bril V, Orszag A, et al. Reproducibility of in vivo corneal confocal microscopy as a novel screening test for early diabetic sensorimotor polyneuropathy. Diabet Med 2011;28:1253-1260
8. Tavakoli M, Kallinikos P, Iqbal A, et al. Corneal confocal microscopy detects improvement in corneal nerve morphology with an improvement in risk factors for diabetic neuropathy. Diabet Med 2011;28:1261-1267
9. Tavakoli M, Mitu-Pretorian M, Petropoulos IN, et al. Corneal confocal microscopy detects early nerve regeneration in diabetic neuropathy after simultaneous pancreas and kidney transplantation. Diabetes 2013;62:254-260
10. Tavakoli M, Quattrini C, Abbott C, et al. Corneal confocal microscopy: a novel noninvasive test to diagnose and stratify the severity of human diabetic neuropathy. Diabetes Care 2010;33:1792-1797
11. Ahmed A, Bril V, Orszag A, et al. Detection of diabetic sensorimotor polyneuropathy by corneal confocal microscopy in type 1 diabetes: a concurrent validity study. Diabetes Care 2012;35:821-828
12. Quattrini C, Tavakoli M, Jeziorska M, et al. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 2007;56:2148-2154 (Pubitemid 47195833)
13. Vagenas D, Pritchard N, Edwards K, et al. Optimal image sample size for corneal nerve morphometry. Optom Vis Sci 2012;89:812-817
14. Turuwhenua JT, Patel DV, McGhee CN. Fully automated montaging of laser scanning in vivo confocal microscopy images of the human corneal subbasal nerve plexus. Invest Ophthalmol Vis Sci 2012;53:2235-2242
15. Allgeier S, Zhivov A, Eberle F, et al. Image reconstruction of the subbasal nerve plexus with in vivo confocal microscopy. Invest Ophthalmol Vis Sci 2011;52:5022-5028
16. Zhivov A, Winter K, Hovakimyan M, et al. Imaging and quantification of subbasal nerve plexus in healthy volunteers and diabetic patients with or without retinopathy. PLoS ONE 2013;8:e52157
17. Köhler B, Allgeier S, Eberle F, et al. [Image reconstruction of the corneal subbasal nerve plexus with extended field of view from focus image stacks of a confocal laser scanning microscope]. Klin Monatsbl Augenheilkd 2011;228:1060-1066
18. Ziegler D, Papanas N, Roden M; GDC Study Group. Neuropad: evaluation of three cut-off points of sudomotor dysfunction for early detection of polyneuropathy in recently diagnosed diabetes. Diabet Med 2011;28:1412-1415
19. Ziegler D, Mayer P, Gries FA. Evaluation of thermal, pain, and vibration sensation thresholds in newly diagnosed type 1 diabetic patients. J Neurol Neurosurg Psychiatry 1988;51:1420-1424 (Pubitemid 18262966)
20. Papanas N, Vinik AI, Ziegler D. Neuropathy in prediabetes: does the clock start ticking early? Nat Rev Endocrinol 2011;7:682-690
21. Bongaerts BW, Rathmann W, Kowall B, et al. Postchallenge hyperglycemia is positively associated with diabetic polyneuropathy: the KORA F4 study. Diabetes Care 2012;35:1891-1893
22. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2012;35(Suppl. 1):S64-S71
23. Winter K, Zhivov A, Guthoff RF, Köhler B, Stachs O. Characteristic quantities for the quantification of CLSM images of the subbasal nerve plexus. Biomed Tech (Berl) 2010;55(Suppl. 1):252-254
24. Ziegler D, Siekierka-Kleiser E, Meyer B, Schweers M. Validation of a novel screening device (NeuroQuick) for quantitative assessment of small nerve fiber dysfunction as an early feature of diabetic polyneuropathy. Diabetes Care 2005;28:1169-1174 (Pubitemid 40616630)
25. Young MJ, Boulton AJ, MacLeod AF, Williams DR, Sonksen PH. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993;36:150-154 (Pubitemid 23034314)
26. McCarthy BG, Hsieh ST, Stocks A, et al. Cutaneous innervation in sensory neuropathies: evaluation by skin biopsy. Neurology 1995;45:1848-1855 (Pubitemid 27122956)
27. Lauria G, Cornblath DR, Johansson O, et al.; European Federation of Neurological Societies. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol 2005;12:747-758 (Pubitemid 41495131)
28. Lauria G, Bakkers M, Schmitz C, et al. Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. J Peripher Nerv Syst 2010;15:202-207
29. Ziegler D, Laux G, Dannehl K, et al. Assessment of cardiovascular autonomic function: age-related normal ranges and reproducibility of spectral analysis, vector analysis, and standard tests of heart rate variation and blood pressure responses. Diabet Med 1992;9:166-175
30. Sivaskandarajah GA, Halpern EM, Lovblom LE, et al. Structure-function relationship between corneal nerves and conventional small-fiber tests in type 1 diabetes. Diabetes Care 2013;36:2748-2755
31. Messmer EM, Schmid-Tannwald C, Zapp D, Kampik A. In vivo confocal microscopy of corneal small fiber damage in diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 2010;248:1307-1312
32. Nitoda E, Kallinikos P, Pallikaris A, et al. Correlation of diabetic retinopathy and corneal neuropathy using confocal microscopy. Curr Eye Res 2012;37:898-906
33. Petropoulos IN, Alam U, Fadavi H, et al. Corneal nerve loss detected with corneal confocal microscopy is symmetrical and related to the severity of diabetic polyneuropathy. Diabetes Care 2013;36:3646-3651
34. Edwards K, Pritchard N, Vagenas D, Russell A, Malik RA, Efron N. Utility of corneal confocal microscopy for assessing mild diabetic neuropathy: baseline findings of the LANDMark study. Clin Exp Optom 2012;95:348-354
35. Quattrini C, Jeziorska M, Boulton AJ, Malik RA. Reduced vascular endothelial growth factor expression and intra-epidermal nerve fiber loss in human diabetic neuropathy. Diabetes Care 2008;31:140-145
36. Sytze Van Dam P, Cotter MA, Bravenboer B, Cameron NE. Pathogenesis of diabetic neuropathy: focus on neurovascular mechanisms. Eur J Pharmacol 2013;719:180-186
37. Bonini S, Rama P, Olzi D, Lambiase A. Neurotrophic keratitis. Eye (Lond) 2003;17:989-995 (Pubitemid 37541053)
38. Ferrari G, Hajrasouliha AR, Sadrai Z, Ueno H, Chauhan SK, Dana R. Nerves and neovessels inhibit each other in the cornea. Invest Ophthalmol Vis Sci 2013;54:813-820
39. Ropper AH, Gorson KC, Gooch CL, et al. Vascular endothelial growth factor gene transfer for diabetic polyneuropathy: a randomized, double-blinded trial. Ann Neurol 2009;65:386-393
40. Zou C, Wang S, Huang F, Zhang YA. Advanced glycation end products and ultrastructural changes in corneas of long-term streptozotocin-induced diabetic monkeys. Cornea 2012;31:1455-1459
41. Spijkerman AM, Dekker JM, Nijpels G, et al. Microvascular complications at time of diagnosis of type 2 diabetes are similar among diabetic patients detected by targeted screening and patients newly diagnosed in general practice: the Hoorn screening study. Diabetes Care 2003;26:2604-2608 (Pubitemid 37052107)